Effects of Probiotics, Prebiotics, and Synbiotics on Human Health
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nutrients Review Effects of Probiotics, Prebiotics, and Synbiotics on Human Health Paulina Markowiak * and Katarzyna Sli´ zewska˙ * Institute of Fermentation Technology and Microbiology, Department of Biotechnology and Food Sciences, Lodz University of Technology, 90-924 Łód´z,Poland * Correspondence: [email protected] (P.M.); [email protected] (K.S.);´ Tel.: +48-42-6313-481 (P.M. & K.S.)´ Received: 24 July 2017; Accepted: 12 September 2017; Published: 15 September 2017 Abstract: The human gastrointestinal tract is colonised by a complex ecosystem of microorganisms. Intestinal bacteria are not only commensal, but they also undergo a synbiotic co-evolution along with their host. Beneficial intestinal bacteria have numerous and important functions, e.g., they produce various nutrients for their host, prevent infections caused by intestinal pathogens, and modulate a normal immunological response. Therefore, modification of the intestinal microbiota in order to achieve, restore, and maintain favourable balance in the ecosystem, and the activity of microorganisms present in the gastrointestinal tract is necessary for the improved health condition of the host. The introduction of probiotics, prebiotics, or synbiotics into human diet is favourable for the intestinal microbiota. They may be consumed in the form of raw vegetables and fruit, fermented pickles, or dairy products. Another source may be pharmaceutical formulas and functional food. This paper provides a review of available information and summarises the current knowledge on the effects of probiotics, prebiotics, and synbiotics on human health. The mechanism of beneficial action of those substances is discussed, and verified study results proving their efficacy in human nutrition are presented. Keywords: probiotic bacteria; prebiotics; synbiotics; human health; gut microbiota 1. Introduction Nowadays, besides the basic role of nutrition consisting in the supply of necessary nutrients for growth and development of the organism, some additional aspects are becoming increasingly important, including the maintenance of health and counteracting diseases. In the world of highly processed food, particular attention is drawn to the composition and safety of consumed products. The quality of food is very important because of, i.e., the problem of food poisoning, obesity, allergy, cardiovascular diseases, and cancer—the plague of the 21st century. Scientific reports point to the health benefits of using probiotics and prebiotics in human nutrition. The word “probiotic” comes from Greek, and it means “for life”. Most probably, it was Ferdinand Vergin who invented the term “probiotic” in 1954, in his article entitled “Anti-und Probiotika” comparing the harmful effects of antibiotics and other antibacterial agents on the intestinal microbiota with the beneficial effects (“probiotika”) of some useful bacteria [1]. Some time after that, in 1965, Lilly and Stillwell described probiotics as microorganisms stimulating the growth of other microorganisms [2]. The definition of probiotics has been modified and changed many times. To emphasise their microbial origin, Fuller (1989) stated that probiotics must be viable microorganisms and must exert a beneficial effect on their host [3]. On the other hand, Guarner and Schaafsma (1998) indicated the necessary use of an appropriate dose of probiotic organisms required to achieve the expected effect [4]. The current definition, formulated in 2002 by FAO (Food and Agriculture Organization of the United Nations) and WHO (World Health Organization) working group experts, states that probiotics are “live strains Nutrients 2017, 9, 1021; doi:10.3390/nu9091021 www.mdpi.com/journal/nutrients Nutrients 2017, 9, 1021 2 of 30 of strictly selected microorganisms which, when administered in adequate amounts, confer a health benefit on the host” [5]. The definition was maintained by the International Scientific Association for Probiotics and Prebiotics (ISAPP) in 2013 [6]. Results of clinical studies confirm the positive effect of probiotics on gastrointestinal diseases (e.g., irritable bowel syndrome, gastrointestinal disorders, elimination of Helicobacter, inflammatory bowel disease, diarrhoeas) and allergic diseases (e.g., atopic dermatitis). Many clinical studies have proven the effectiveness of probiotics for treatment of diseases such as obesity, insulin resistance syndrome, type 2 diabetes, and non-alcoholic fatty liver disease. Furthermore, the positive effects of probiotics on human health have been demonstrated by increasing the body’s immunity (immunomodulation). Scientific reports also show the benefits of the prophylactic use of probiotics in different types of cancer and side effects associated with cancer. Many clinical studies have proven the effectiveness of probiotics, and recommended doses of probiotics are those that have been used in a particular case. Keep in mind that how probiotics work may depend on the strain, dose, and components used to produce a given probiotic product. In 1995, prebiotics were defined by Gibson and Roberfroid as non-digested food components that, through the stimulation of growth and/or activity of a single type or a limited amount of microorganisms residing in the gastrointestinal tract, improve the health condition of a host [7]. In 2004, the definition was updated and prebiotics were defined as selectively fermented components allowing specific changes in the composition and/or activity of microorganisms in the gastrointestinal tract, beneficial for host’s health and wellbeing [8]. Finally, in 2007, FAO/WHO experts described prebiotics as a nonviable food component that confers a health benefit on the host associated with modulation of the microbiota [9]. Prebiotics may be used as an alternative to probiotics or as an additional support for them. However different prebiotics will stimulate the growth of different indigenous gut bacteria. Prebiotics have enormous potential for modifying the gut microbiota, but these modifications occur at the level of individual strains and species and are not easily predicted a priori. There are many reports on the beneficial effects of prebiotics on human health. High potential is attributed to the simultaneous use of probiotics and prebiotics. In 1995, Gibson and Roberfroid introduced the term “synbiotic” to describe a combination of synergistically acting probiotics and prebiotics [7]. A selected component introduced to the gastrointestinal tract should selectively stimulate growth and/or activate the metabolism of a physiological intestinal microbiota, thus conferring beneficial effect to the host’s health [10]. As the word “synbiotic” implies synergy, the term should be reserved for those products in which a prebiotic component selectively favours a probiotic microorganism [11]. The principal purpose of that type of combination is the improvement of survival of probiotic microorganisms in the gastrointestinal tract. Synbiotics have both probiotic and prebiotic properties and were created in order to overcome some possible difficulties in the survival of probiotics in the gastrointestinal tract [12]. Therefore, an appropriate combination of both components in a single product should ensure a superior effect, compared to the activity of the probiotic or prebiotic alone [13,14]. The aim of the review was to discuss the mechanisms of action of probiotics, prebiotics, and synbiotics, as well as the current insight into their effect on human health. The selection of probiotic strains, prebiotics, and their respective dosages is crucial in obtaining a therapeutic effect, so separate sections are dedicated to this topic. Further research into the acquisition of new probiotic strains, the selection of probiotics and prebiotics for synbiotics, dose setting, safety of use, and clinical trials documenting the desired health effects is necessary. Effects should be confirmed in properly scheduled clinical trials conducted by independent research centres. 2. Probiotics The knowledge of the beneficial effects of lactic acid fermentation on human health dates back to ancient times. The Bible mentions sour milk several times. Ancient Romans and Greeks knew various Nutrients 2017, 9, 1021 3 of 30 recipes for fermented milk. A specific type of sour milk, called “leben raib”, prepared from buffalo, cow, or goat milk, was consumed in ancient Egypt. A similar “jahurt” was also commonly consumed by people inhabiting the Balkans. In India, fermented milk drinks were known already 800–300 years B.C., and in Turkey in the 8th century. A milk drink called “ajran” was consumed in Central Russia in the 12th century, and “tarho” was consumed in Hungary in the 14th century [15]. A particular interest in lactic acid fermentation was expressed in the beginning of the 20th century by the Russian scientist and immunologist working for the Pasteur Institute in Paris, awarded with the Nobel Prize in medicine for his work on immunology (in 1907), Ilia Miecznikow. Here is a quote from his book “Studies on Optimism”: “with various foods undergoing lactic acid fermentation and consumed raw (sour milk, kefir, sauerkraut, pickles) humans introduced huge amounts of proliferating lactic acid bacteria to their alimentary tracts” [16]. 2.1. Selection Criteria and Requirements for Probiotic Strains According to the suggestions of the WHO, FAO, and EFSA (the European Food Safety Authority), in their selection process, probiotic strains must meet both safety and functionality criteria, as well as those related to their technological